Expression of pair rule gene orthologs in the blastoderm of a myriapod: evidence for pair rule-like mechanisms?
© Janssen et al.; licensee BioMed Central Ltd. 2012
Received: 17 October 2011
Accepted: 11 April 2012
Published: 17 May 2012
A hallmark of Drosophila segmentation is the stepwise subdivision of the body into smaller and smaller units, and finally into the segments. This is achieved by the function of the well-understood segmentation gene cascade. The first molecular sign of a segmented body appears with the action of the pair rule genes, which are expressed as transversal stripes in alternating segments. Drosophila development, however, is derived, and in most other arthropods only the anterior body is patterned (almost) simultaneously from a pre-existing field of cells; posterior segments are added sequentially from a posterior segment addition zone. A long-standing question is to what extent segmentation mechanisms known from Drosophila may be conserved in short-germ arthropods. Despite the derived developmental modes, it appears more likely that conserved mechanisms can be found in anterior patterning.
Expression analysis of pair rule gene orthologs in the blastoderm of the pill millipede Glomeris marginata (Myriapoda: Diplopoda) suggests that these genes are generally involved in segmenting the anterior embryo. We find that the Glomeris pairberry-1 ( pby-1) gene is expressed in a pair rule pattern that is also found in insects and a chelicerate, the mite Tetraynchus urticae. Other Glomeris pair rule gene orthologs are expressed in double segment wide domains in the blastoderm, which at subsequent stages split into two stripes in adjacent segments.
The expression patterns of the millipede pair rule gene orthologs resemble pair rule patterning in Drosophila and other insects, and thus represent evidence for the presence of an ancestral pair rule-like mechanism in myriapods. We discuss the possibilities that blastoderm patterning may be conserved in long-germ and short-germ arthropods, and that a posterior double segmental mechanism may be present in short-germ arthropods.
In Drosophila, a hierarchic segmentation gene cascade acts to stepwise pattern the early embryo into single segments (reviewed in [1–3]). Maternally provided factors such as bicoid and hunchback, rest at the top of this hierarchy, which allows these genes to regulate zygotically expressed gap genes (GGs) (, reviewed in ). The GGs, that are expressed in broad overlapping domains along the anterior-posterior axis of the embryo, regulate the pair rule genes (PRGs) in transversal stripes in alternating segment primordia . During a subsequent phase of segment formation, the PRGs are often expressed in a single segmental periodicity and, at this point, act as segment-polarity genes (SPGs) (e.g. [7, 8]). In a combinatorial mode the PRGs regulate the expression of the SPGs, which maintain the parasegment boundaries and define the segments’ polarity.
This mode of segment formation is called long-germ developmental mode because all segments are patterned from a pre-existing field of cells, the blastoderm (e.g. ). Drosophila development, however, is derived, and is, at best, comparable to some groups of higher insects. Only the most anterior segments form from the blastoderm in the majority of arthropods, while the posterior segments are added in a single or double segment period from a posterior segment addition zone (SAZ) . This ancestral mode of development and segment formation is called short-germ developmental mode.
Recent studies have shown that the mechanisms and gene interactions acting at the bottom level of the Drosophila segmentation gene cascade, i.e. SPGs and Hox genes, appear to be highly conserved among arthropods (e.g. [11–15]) and onychophorans [16, 17]. At the level of maternally provided effect genes and GGs, however, the segmentation gene hierarchy appears to be less conserved (e.g. ). The level at which the PRGs act is intermediate between that of the SPGs and Hox genes, and that of maternally provided effect genes and GGs (e.g. ). Examination of PRG expression and function in insects other than Drosophila revealed that this level of the segmentation gene cascade is, to some degree, conserved in insects (e.g. [19–21]). The expression profile of PRGs in most insects is, however, somewhat different from that in Drosophila. In non-Drosophilid long-germ insects, PRGs are often initially expressed in double-segment wide stripes that later split into a single segmental pattern (e.g. [22, 23]). In short-germ insects a similar pattern is found in the anterior blastoderm, but during posterior segment addition PRGs are, like in non-insect arthropods, usually expressed in both dynamic patterns in the SAZ and in stripes in the newly formed segment(s) (e.g. [14, 24–28]). It is therefore debatable whether they are involved in a pair rule-like mechanism (e.g. [2, 18, 29]). Data on early PRG expression or function in the blastoderm in non-insect arthropods are scant [30, 31] and for that reason, it is unclear whether a pair rule-like mechanism may be present in anterior patterning.
To shed light on this topic we examined the expression of most of the known Drosophila PRG orthologs in the blastoderm of the pill millipede Glomeris marginata (Myriapoda). The orthologs of two Drosophila PRG genes are not subject of this study: The fushi-tarazu gene acts as a classical PRG in Drosophila, but in basal hexapods and other arthropods, including Glomeris, it may have retained its ancestral role as Hox gene and does not act as a PRG [25, 32–34]. The tenascin-major ( ten-m) gene (aka odz) is a rather atypical PRG in Drosophila. It does not encode a transcription factor, like all other PRGs, and only has been student in Drosophila where it is only expressed in a pair rule pattern on protein level, but not on mRNA level. Therefore we decided not to include ten-m in the present analysis. We find that all investigated PRG orthologs, except one, are expressed in transversal stripes that are typical for segmentation genes and which are in patterns that may be in accord with an underlying pair rule-like mechanism. The blastodermal expression of the PRGs is different from that in segments added from the SAZ in Glomeris: they do not appear in a strict anterior to posterior order and are often initially expressed in double (or multiple) segment-wide domains.
Species husbandry, gene cloning, in situ hybridization, nuclei staining and documentation techniques
The handling of Glomeris marginata is described in . After oviposition, embryos were allowed to develop at room temperature. Staging was done afterwards . The developmental stage of all embryos was determined by using the dye, DAPI (4'-6-Diamidino-2-phenylindole).
Cloning and sequence analysis of the Glomeris pair rule gene orthologs has been described in .
Embryos were analyzed under a Leica dissection microscope equipped with either an Axiocam (Zeiss) or a Leica DC100 digital camera. Brightness, contrast, and color values were corrected in all images using the image processing software Adobe Photoshop CS2 (Version 9.0.1 for Apple Macintosh).
Morphology of the early Glomerisembryo and technical limitations of in situ hybridization experiments
Currently, it is not possible to perform mRNA detection studies (in situ hybridization) in embryos younger than stage 0. At this stage the inner vitelline membrane forms in Glomeris. Attempts to fix embryos at earlier developmental stages (representing development from one to six days at room temperature) in the absence of a functional vitelline membrane, have failed.
Expression of even-skipped ( eve) in the regio germinalis
In Drosophila the eve gene is under control of the upstream acting maternal effect genes and gap genes, and each of the seven transversal stripes of early eve-expression becomes specified separately by disjoined enhancer elements (e.g. [38–40]). Because of this direct control of eve by the upstream level segmentation genes it represents a primary PRG. One of its important functions during early development in Drosophila is to indirectly regulate the segment polarity gene engrailed by regulating its activators paired and fushi-tarazu and its repressors runt and sloppy paired. The crucial function of eve among the PRGs is also conserved in other insects such as Tribolium[20, 42] and Gryllus, but may be different in other insects (e.g. ).
Expression of runt (run) in the regio germinalis
Like eve, also run acts as a primary PRG in Drosophila where one of its key functions is to regulate other PRGs as well as primary upstream acting gap genes (GGs) and maternal effect genes. In Drosophila run is thus an important component of the cross regulatory network of PRGs, GGs and maternal effect genes . The important function of run in the pair rule regulatory network is conserved in short germ insects as well .
Expression of hairy-1 (h1) in the regio germinalis
Expression of the second Glomeris hairy ortholog, h2, appears in transversal stripes at stage 0.1 in the mandibular, maxillary and T1 segments and weakly in the SAZ (Figure 4L). Later, expression in the postmaxillary segment appears. Expression in the mandibular and the maxillary segment broadens and expression corresponding to the T3 stripe forms in the anterior SAZ (Figure 4N). Double staining shows that h2 is expressed anterior and adjacent to the segment polarity gene engrailed ( en) (Figure 4O and Additional file 1: Figure S1B).
Expression of sloppy-paired ( slp) in the regio germinalis
In the fly Drosophila and the beetle Tribolium slp acts as a secondary PRG and is in these species regulated by the primary PRGs . In Drosophila it acts as a gap gene in the head segments and a pair rule like regulator of SPGs in the trunk segments where it functions as an activator of wingless ( wg) and as a repressor of engrailed ( en) [8, 49].
Expression of pairberry-1 (pby-1) in the regio germinalis
In Drosophila the paired ( prd) gene is classified as a so-called tertiary PRG because it functions at the lowest level of the pair rule gene cascade as a direct activator of wingless ( wg) and engrailed ( en) . Expression and functional analysis of paired orthologs in other insects revealed that its function is conserved among insects (e.g. [51, 52]).
Double staining with engrailed ( en) reveals that pby-1 is expressed anterior to en in anterior segments that have formed from the regio germinalis (Additional file 1: Figure S1D). Both genes also appear to be co-expressed in one row of cells, but this is not unambiguously clear from the available expression data (Additional file 1: Figure S1D). The intrasegmental expression of pby-1 is conserved in anterior and posterior segments (cf. ), and this is consistent with a conserved regulatory function of pby-1 in segment polarity gene regulation.
Expression of odd-paired ( opa) and odd-skipped ( odd) in the regio germinalis
In Drosophila opa acts as a secondary PRG. An oddity of opa is that it is not expressed in the typical striped pattern as all the other PRGs, but it is expressed ubiquitously in the centre of the early embryo. Its presence is required but not instructive for the regulation of segment polarity genes [7, 54]. In Tribolium opa is expessed in stripes but does not act as a pair rule gene .
Interestingly, in Drosophila the odd gene is historically considered as a secondary PRG that is under control of the primary PRGs, and is repressed by eve. In Tribolium, however, odd is part of the high-level regulatory circuit that controls secondary PRGs, and even represses eve. Based on the find that odd expression is regulated through stripe specific elements, recently it has been suggested that Drosophila odd should rather be considered as a primary than a secondary PRG . Furthermore also expression pattern analysis in another myriapod, the centipede Strigamia, suggests an important role for an odd-related gene in this species .
In Glomeris the odd gene is initially expressed in the most anterior area of the developing embryo, while being weakly expressed in the future T1, the SAZ and its posterior pole (Figure 7D). At stage 0.5 the anterior domain is restricted to a central position. Two patches of expression are located dorsal and posterior to this domain. The affiliation of this expression is unclear, but is possibly within future antennal, premandibular and mandibular tissue (Figure 7E). Faint expression is visible in developing segments between this domain and T1. Three stripes of expression appear posterior to T1 representing expression in the future segments T2 to T4 (Figure 7E). Altogether, the expression pattern of odd is not indicative for a pronounced role during the formation/patterning of segments that form from the regio germinalis. This implies that it does not play such a crucial role in the segmentation process in this myriapod as it does in long and short germ insects and a centipede. In segments that arise from the posterior segment addition zone (SAZ), however, Glomeris odd is prominently expressed in the SAZ itself and subsequently also in the dorsal segmental units . This on the other hand suggests fundamental differences between the patterning of anterior vs posterior segments.
Other PRG orthologs, i.e. the paralogs pairberry-2 ( pby2) and hairy-3 ( h3) are not expressed in early stages in the regio germinalis.
The Glomeris pby-1gene is expressed in a pattern reminiscent of that of classical PRGs
An important question that must be addressed is whether PRG orthologs may be involved in a pair rule-like mechanism during segment formation and if this is comparable to that found in the model organism, Drosophila (e.g.[2, 18]).
The early expression of prd/pby orthologs has also been examined in other insect species than Drosophila. In the wasp, Nasonia vitripennis, a long-germ insect, like Drosophila, stripes of prd expression appear in an anterior to posterior progression with every other stripe being weaker. Whether this is a result of splitting stripes like in Drosophila is unclear from the present data . In the short-germ insect, Tribolium, broad stripes of prd expression appear that soon after split . Notably, the maxillary stripe is weaker than the mandibular and labial stripes. With the elongation of the germ band, additional stripes of prd expression appear in the anterior of the SAZ that later split into expression in T1+T2, T3+A1 et cetera. Importantly, in Tribolium prd acts as a true PRG with a clear pair rule phenotype setting an example that splitting domains of double-segment wide initial expression patterns can be functionally comparable to Drosophila pair rule patterning [20, 51]. In the hemimetabolous short-germ insect, Schistocerca americana, the mandibular and labial stripes of prd expression first appear together with a broad posterior domain that gives rise to expression in the second and third thoracic segment. With some delay weaker stripes in between (in the maxillary and the first thoracic segment) appear [3, 53]. Notably, the mandibular stripe does not appear as a separate stripe but is the result of a broad splitting domain covering the gnathal arc that transforms also into the labial stripe .
The early pattern in long-germ and short-germ insects is therefore similar. Stripes form as broad double-segment wide domains that then split giving rise to the secondary pattern of prd expression (Figure 8). The result is often a secondary expression pattern with strong and weak prd/ pby expression in alternating segments (Figure 8), which is the pattern also present in Glomeris.
Interestingly, the same early expression profile of prd orthologs has also been described for the spider mite, Tetraynchus urticae (Chelicerata), where the paired ortholog, Tu-pax3/7, is initially expressed in alternating segments in the anterior body. In somewhat later stages, expression of Tu-pax3/7 appears in the interjacent segments . This pattern is virtually identical to that of Glomeris pby-1 except the expression patterns of the first and third walking leg bearing segments (= mandibular and postmaxillary segments in Glomeris) in the mite are clearly delayed (Figure 8). This finding, if not caused by convergence, may place the origin of the expression pattern of prd orthologs (and possibly also its early function) at the very base of the Arthropoda.
The early strong expression of Tu-pax3/7 is in the same (homologous) segments as the strong expression in Glomeris, but the location of the primary (stronger) prd/ pby-stripes in insects is shifted by one segment towards posterior (Figure 8). Since the homology of arthropod head segments appears to be solidly resolved by brain innervation patterns (e.g. [58, 59]) and Hox gene expression patterns (e.g. [17, 32, 60, 61]), this difference must be the result of different regulation of prd/ pby genes in the different arthropod classes.
Expression of PRGs in double-segment wide domains: a feature of pair rule function?
It is possible that the splitting of double-segment wide expression domains is an ancestral regulatory feature of arthropod PRGs, because it is present in the blastoderm of insects, a myriapod (this study) and also a spider .
Initial expression of PRGs in broad domains may be a genetic constraint, because their early expression patterns are likely to be regulated by the gap-genes (GGs), as known from insects (e.g. [23, 62–65]). Since the GGs are expressed in broad domains they may activate PRGs that are also initially located in broad domains, but that then transform into segmental stripes, possibly by the combinatorial action of the PRGs themselves.
Blastoderm patterning in long- and short-germ arthropods
In the model arthropod, Drosophila melanogaster, all segments are patterned at the blastoderm stage. This, however, represents a derived developmental mode, and hence the segmentation gene cascade known to act in Drosophila cannot function in the same way in short-germ arthropods that add posterior segments sequentially from a posterior SAZ (e.g. ).
Functional studies and gene expression analysis have shown that the PRGs are likely to be involved in segment formation in non-insect arthropods (e.g. [24–26, 55, 67, 68]). Despite that, it was largely unclear whether PRGs are also involved in anterior patterning in non-insect arthropods, as only very few studies examine PRG function and/or expression at early blastoderm stages in non-insect arthropods [30, 31].
The data presented here suggest that most of the investigated PRGs in Glomeris are involved in segmental patterning of the blastoderm. All PRGs (except odd-skipped) are expressed in transversal stripes corresponding to one or multiple segment primordia (discussed above). Expression of any given PRG does not appear simultaneously or in an anterior posterior order, but with minimal temporal variance in different segmental primordia. Furthermore, the order of appearance of the segmental primordia differs for every PRG ortholog (Figure 9). This is comparable to what happens in Drosophila, where the PRGs often appear in an irregular progression in the blastoderm and the initial expression is often in broad domains and not in the classical seven-stripe pattern (e.g. [54, 56, 69]).
The stereotypic appearance of the PRGs in the regio germinalis in Glomeris is superficially reflected by the appearance of the SPG en. en transcription starts later compared to when most of the PRGs are transcribed, which is in accord with a possible regulatory function of some of the PRGs on en in the anterior embryo in Glomeris. While the PRGs appear to be active before the onset of the SPGs  and the expression of the Hox genes , the anterior acting GGs are expressed as early as, or possibly earlier .
The principal hierarchy of segmentation gene interaction known from Drosophila with GGs regulating PRGs and PRGs regulating SPGs can be conserved in Glomeris as well, at least with respect to segment formation in the blastoderm.
It is tempting to speculate that anterior patterning is indeed conserved among long- and short-germ arthropods and that this possibly ancestral patterning mechanism has been extended to the complete embryo in Drosophila and other long-germ insects. Results of this transition may have been the recruitment of the posterior acting GGs and the loss of the posterior segmentation clock as suggested by .
Pair rule-like mechanism in posterior segment addition?
Patterning of segments in pairs may be an ancestral mechanism (discussed above). The dynamic expression of some PRGs in the posterior SAZ in myriapods [14, 24, 55, 68] may be the equivalent of double-segment wide stripes of PRGs in the blastoderm. This condition is most evident in the centipede, Strigamia, where the addition of posterior segments occurs in pairs and with the involvement of PRGs, such as even-skipped, from the posterior SAZ . Further evidence for this hypothesis comes from centipedes where the number of trunk segments is always odd (reviewed in [72, 73]). This shows that there may be a genetic constraint that does not allow for the formation of an even number of trunk segments in centipedes .
Furthermore, in Glomeris the number of trunk segments is always 17 for females and 19 for males. This indicates that the posterior segmentation clock in Glomeris males may produce another two segments by adding one cycle of dynamic gene expression during its development.
We have found evidence, in the form of gene expression patterns, that Drosophila pair rule gene orthologs are also likely involved in anterior body patterning in the myriapod Glomeris marginata. This finding, however, requires further investigation through functional studies, which, at the moment, have not yet been established for Glomeris, or any other myriapod species. The expression patterns found in Glomeris are, to some extent, similar, and thus reminiscent of true pair rule patterning as seen in Drosophila. Comprehensive comparative expression data from other arthropods, and especially crustaceans, are necessary to gain a better understanding of the ancestral mode(s) of arthropod segmentation.
This work has been supported by the Swedish Research Council (VR: grant to GEB), the European Union via the Marie Curie Training network “ZOONET” (MRTN-CT-2004-005624 (to GEB, WGMD and RJ)) and the DFG via SFB 572 of the University of Cologne (to WGMD and RJ).
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